Bird predation selects for wing shape and coloration in a damselfly

Wing shape is related to flight performance, which is expected to be under selection for improving flight behaviours such as predator avoidance. Moreover, wing conspicuousness, usually involved in sexual selection processes, is also relevant in terms of predation risk. In this study, we examined how predation by a passerine bird, the white wagtail Motacilla alba, selects wing shape and wing colour patch size in males of the banded demoiselle Calopteryx splendens. The wing colour patch is intra‐ and intersexually selected in the study species. In a field study, we compared wings of live damselflies to wings of predated damselflies which are always discarded after predation. Based on aerodynamic theory and a previous study on wing shape of territorial tactics in damselflies, we predicted an overall short and broad wing, with a concave front margin shape to be selected by predation. This shape would be expected to improve escaping ability. Moreover, we predicted that wing patch size should be negatively selected by predation. We found that selection operated differently on fore‐ and hindwings. In contrast to our predictions, predation favoured a slender general forewing shape. However, the predicted wing shape was favoured in hindwings. We also found selection favouring a narrower wing colour patch. Our results suggest different roles of fore‐ and hindwings in flight, as previously suggested for Calopteryx damselflies and shown for butterflies and moths. Forewings would be more involved in sustained flight and hindwings in flight manoeuvrability. Our results differ somehow from a recently published work in the same study system, but using another population, suggesting that selection can fluctuate across space, despite the simplicity of this predator–prey system.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

Habitat variation and wing coloration affect wing shape evolution in dragonflies

Habitats are spatially and temporally variable, and organisms must be able to track these changes. One potential mechanism for this is dispersal by flight. Therefore, we would expect flying animals to show adaptations in wing shape related to habitat variation. In this work, we explored variation in wing shape in relation to preferred water body (flowing water or standing water with tolerance for temporary conditions) and landscape (forested to open) using 32 species of dragonflies of the genus Trithemis (80% of the known species). We included a potential source of variation linked to sexual selection: the extent of wing coloration on hindwings. We used geometric morphometric methods for studying wing shape. We also explored the phenotypic correlation of wing shape between the sexes. We found that wing shape showed a phylogenetic structure and therefore also ran phylogenetic independent contrasts. After correcting for the phylogenetic effects, we found (i) no significant effect of water body on wing shape; (ii) male forewings and female hindwings differed with regard to landscape, being progressively broader from forested to open habitats; (iii) hindwings showed a wider base in wings with more coloration, especially in males; and (iv) evidence for phenotypic correlation of wing shape between the sexes across species. Hence, our results suggest that natural and sexual selection are acting partially independently on fore‐ and hindwings and with differences between the sexes, despite evidence for phenotypic correlation of wing shape between males and females.     

The effects of latitude,body size,and sexual selection on wing shape in a damselfly

Under natural selection, wing shape is expected to evolve to optimize flight performance. However, other selective factors besides flight performance may influence wing shape. One such factor could be sexual selection in wing sexual ornaments, which may lead to alternative variations in wing shape that are not necessarily related to flight performance. In the present study, we investigated wing shape variations in a calopterygid damselfly along a latitudinal gradient using geometric morphometrics. Both sexes show wing pigmentation, which is a known signal trait at intra‐ and interspecific levels. Wing shape differed between sexes and, within the same sex, the shape of the hind wing differed from the front wing. Latitude and body size explained a high percentage of the variation in wing shape for female front and hind wings, and male front wings. In male hind wings, wing pigmentation explained a high amount of the variation in wing shape. On the other hand, the variation in shape explained by pigmentation was very low in females. We suggest that the conservative morphology of front wings is maintained by natural selection operating on flight performance, whereas the sex‐specific differences in hind wings most likely could be explained by sexual selection. The observed sexual dimorphism in wing shape is likely a result of different sex‐specific behaviours. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 263–274.     

Sexual selection on flight endurance,flight-related morphology and physiology in a scrambling damselfly

We have limited knowledge on the mechanistic base of sexual selection, especially in scrambling species. This asks for a functional approach that explores the link between each component of the phenotype-performance-fitness axis and that includes both morphological and physiological traits. We explored the phenotype-performance-fitness axis in the scrambling damselfly Coenagrion puella by studying the links between a set of physiological and morphological traits, flight performance (flight speed and flight endurance), and short-term mating success. As expected for scrambling competition, there was sexual selection for increased flight endurance rather than for increased flight speed. For fat content, we could demonstrate the full phenotype-performance-fitness axis, where selection for a higher fat content could be explained by the sexual selection for a higher flight endurance and the positive covariation between fat content and flight endurance. For three other traits (size, relative flight muscle mass and wing loading), however, we detected selection that could not be explained via their effect on flight performance, generating novel testable hypotheses about how the covariation between these traits and mating success is generated. This also urges caution when using morphological traits as proxies for flight speed and flight endurance in phenotypic selection studies.     

Residual reproductive value and male mating success: older males do better

Evolution via sexual selection has traditionally been viewed as isolated from life-history constraints. As additionally reproductive resource allocation in males is underexplored, it is rather unclear how life-history factors have shaped lifetime investment into male sexually selected traits. Against this background, we here investigate male butterfly mating success in relation to age, nutritional status, assay condition and wing damage. As predicted, based on a low residual reproductive value, older males had a considerably higher mating success than younger males. Comparisons between virgin and once-mated males suggest that this pattern is related to age per se rather than differential ratings of the resource receptive female. We found no evidence for male body size or condition being important, supporting the notion that in weaponless animals intrinsic motivation is more important for mating success than the differences in physical properties (such as body size or condition). Flight cage experiments suggest that such differences in motivation may be masked under more natural conditions, where flight performance, having a clear impact on mating success (as evidenced by wing manipulation experiments), is likely to be crucial. We conclude that the life-history perspective is a fruitful one for gaining a better understanding of the evolution of sexually selected characters and the predictions derived from contest theory do also apply to male mating success.     

Morphological and physiological sexual selection targets in a territorial damselfly

• 1 Several morphological and physiological traits may shape fitness through the same performance measure. In such cases, differentiating between a scenario of many‐to‐one mapping, where phenotypic traits independently shape fitness leading to functional redundancy, and a scenario where traits strongly covary among each other and fitness, is needed.
• 2 A multivariate approach was used, including morphological and physiological traits related to flight ability, a crucial performance measure in flying insects, to identify independent correlates of short‐term mating success (mated versus unmated males) in the territorial damselfly Lestes viridis.
• 3 Males with higher flight muscle mass, higher relative thorax mass, and more symmetrical hindwings, all traits presumably linked to manoeuvrability, were more likely to be mated. Unexpectedly, although relative thorax mass is often used as a proxy for flight muscle mass, both traits were selected for independently. Mated males had a higher thorax fat content than unmated males, possibly because of enhanced flight endurance.
• 4 The finding of several independent targets of sexual selection linked to flight ability is consistent with a scenario of many‐to‐one mapping between phenotype and performance. Identifying such a scenario is important, because it may clarify situations where animals may show suboptimal values for some phenotypic traits shaping a performance measure, while still having high performance and fitness. We argue in the discussion that the functional approach of sexual selection provides a potent tool for examining unresolved issues in both sexual selection theory, as well as life‐history theory.

     

Mixed support for an alignment between phenotypic plasticity and genetic differentiation in damselfly wing shape

The relationship between genetic differentiation and phenotypic plasticity can provide information on whether plasticity generally facilitates or hinders adaptation to environmental change. Here, we studied wing shape variation in a damselfly (Lestes sponsa) across a latitudinal gradient in Europe that differed in time constraints mediated by photoperiod and temperature. We reared damselflies from northern and southern populations in the laboratory using a reciprocal transplant experiment that simulated time-constrained (i.e. northern) and unconstrained (southern) photoperiods and temperatures. After emergence, adult wing shape was analysed using geometric morphometrics. Wings from individuals in the northern and southern populations differed significantly in shape when animals were reared in their respective native environment. Comparing wing shape across environments, we found evidence for phenotypic plasticity in wing shape, and this response differed across populations (i.e. G × E interactions). This interaction was driven by a stronger plastic response by individuals from the northern population and differences in the direction of plastic wing shape changes among populations. The alignment between genetic and plastic responses depended on the specific combination of population and rearing environment. For example, there was an alignment between plasticity and genetic differentiation under time-constrained, but not under non-time-constrained conditions for forewings. We thus find mixed support for the hypothesis that environmental plasticity and genetic population differentiation are aligned. Furthermore, although our laboratory treatments mimicked the natural climatic conditions at northern and southern latitudes, the effects of population differences on wing shape were two to four times stronger than plastic effects. We discuss our results in terms of time constraints and the possibility that natural and sexual selection is acting differently on fore- and hindwings.     

Maintenance of variation in sexually selected traits in females: a case study using intrasexual aggression in tree swallows Tachycineta bicolor

A fundamental question in evolutionary biology is how phenotypic variation is maintained in the face of selection that ought to deplete that variation. Much research has investigated this question in traits favored via sexual selection in males, with a common solution implicating the condition dependence of sexually selected phenotypes. Despite growing interest in sexual selection on females, it is not clear if the same mechanisms maintain variation in female ornaments, weaponry or other female behaviors targeted by sexual selection. An important step in testing condition dependence in females is thus to identify whether sexually selected female phenotypes are associated with condition and also with potential costs. Here, I examine these two components of condition dependence for a sexually selected behavior, intrasexual aggression, in female tree swallows Tachycineta bicolor. I asked whether high levels of intrasexual aggression map onto natural variation in female condition and whether aggression is associated with one potential behavioral cost: performance in a vertically challenging test of flight. More aggressive females were heavier for their body size, heavier for their wing size and showed decreased flight ability, relative to less aggressive females. These findings are consistent with condition dependence, where only females in better condition are able to be highly aggressive. The association between high aggression and reduced flight ability may result from the additional lift required to power these relatively heavier birds. These associations between natural variation in aggressive behavior, morphology and flight ability are consistent with condition dependence because they confirm two basic assumptions of condition dependence: a link between aggression and condition, and a link between aggression and a behavioral cost, the speed of escape flight. As the first study to examine these assumptions for a conspicuous behavior favored by intrasexual selection in females, this study suggests broad relevance of condition dependence.     

Altitude and life‐history shape the evolution of Heliconius wings

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal‐mating clade are smaller than those in the adult‐mating clade. Interestingly, we find that high‐altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high‐altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration.     

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S. neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male–male competition. We predicted that populations subject to increased male–male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male‐biased SSD in both species, which was not evident in conspecific populations with female‐biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.     

The potential influence of morphology on the evolutionary divergence of an acoustic signal

The evolution of acoustic behaviour and that of the morphological traits mediating its production are often coupled. Lack of variation in the underlying morphology of signalling traits has the potential to constrain signal evolution. This relationship is particularly likely in field crickets, where males produce acoustic advertisement signals to attract females by stridulating with specialized structures on their forewings. In this study, we characterize the size and geometric shape of the forewings of males from six allopatric populations of the black field cricket (Teleogryllus commodus) known to have divergent advertisement calls. We sample from each of these populations using both wild‐caught and common‐garden‐reared cohorts, allowing us to test for multivariate relationships between wing morphology and call structure. We show that the allometry of shape has diverged across populations. However, there was a surprisingly small amount of covariation between wing shape and call structure within populations. Given the importance of male size for sexual selection in crickets, the divergence we observe among populations has the potential to influence the evolution of advertisement calls in this species.     

Origin and transformation of the in‐flight wing‐coupling structure in Psocodea (Insecta: Paraneoptera)

Many four‐winged insects have mechanisms that unite the forewings and hindwings in a single plane. Such an in‐flight wing coupling apparatus may improve flight performance in four‐winged insects, but its structure is variable among different insect groups. The wings of bark lice (Insecta: Psocodea: “Psocoptera”) also have an in‐flight wing coupling apparatus, but to date, its morphology has not been studied in detail. In this study, we examined the wing‐coupling structure in representative species of the three suborders of bark lice (Trogiomorpha, Troctomorpha, and Psocomorpha) and inferred its origin and transformation. We conclude that the main component of the psocodean wing coupling apparatus evolved once in the common ancestor via modification of cuticular structures at the apex of the forewing CuP vein. Morphological differences in components of the coupling structures are phylogenetically informative at the intraorder level and include an autapomorphy that characterizes Troctomorpha and a synapomorphy that supports a sister relationship between Troctomorpha and Psocomorpha.     

Sexual Selection on Accessory Glands, Genitalia and Protarsal Pads in the Whirligig Beetle Dineutus nigrior Roberts (Coleoptera: Gyrinidae)

Sexual selection is a potent force in the evolution of morphology in sexually reproducing species. When large size in a trait is favored by sexual selection the trait often exhibits positive allometry. Mating behavior in whirligig beetles consists of males attempting to grasp reluctant females using enlarged protarsi (protarsal pads). Here we use allometry and a mating experiment to investigate sexual selection pressures on accessory glands, intromittant genitalia (aedeagus), and protarsal pads in males of the whirligig beetle Dineutus nigrior Roberts. Accessory gland size exhibited positive allometry and males with larger accessory glands were more likely to copulate suggesting that larger size in this trait is favored by sexual selection. Males with larger accessory glands attempted to copulate more often but did not exhibit fewer failed mating attempts before copulating. This suggests that the increased probability of mating in males with large accessory glands is due to higher mating attempt frequency and not to increased ability to overcome female resistance. The length of the aedeagus exhibited negative allometry and males with a longer aedeagus did not have increased mating success. This is consistent with stabilizing selection favoring an intermediate size in this trait. The allometric slope of the protarsal pad did not differ from isometry and males with larger protarsal pads did not have increased mating success. This suggests that larger protarsal pads are not favored by sexual selection.     

Codivergence but Limited Covariance of Wing Shape and Calling Song Structure in Field Crickets (<Emphasis Type="Italic">Gryllus</Emphasis>)

Morphological traits are often used in performing ecological tasks or in sexual display behaviour. Variation in morphology is thus expected to be coupled to variation in idiosyncratic behaviours across ecologically or sexually diverged lineages. However, it is poorly understood whether this prediction holds and how functional constraints, shared ancestry, or selection contribute to morphology-behaviour co-evolution. Here, we test this prediction in four cricket species, which differ strikingly in their sexually selected mate calling songs, produced by engaging their specialized forewings. Using geometric morphometrics we provide the first evidence that wing shape and size varies consistently across species. We then test whether wing shape and song co-evolve and whether co-evolution is best explained by individual-level functional/genetic covariance or by population-level evolutionary covariance. Song structure and wing shape are coupled, even after accounting for phylogeny. However, there is limited covariance within species. Thus, wing morphology and sexual signalling behaviour in crickets are likely linked due to shared (ancestral) effects from neutral and selective processes. We show that morphology and behaviour can be linked across but not within species and discuss how evolutionary stasis, genetic linkage, and evolutionary covariance help explain this pattern.     

Evolutionary constraints in hind wing shape in Chinese dung beetles (Coleoptera: Scarabaeinae)

This study examines the evolution hindwing shape in Chinese dung beetle species using morphometric and phylogenetic analyses. Previous studies have analyzed the evolution of wing shape within a single or very few species, or by comparing only a few wing traits. No study has analyzed wing shape evolution of a large number of species, or quantitatively compared morphological variation of wings with proposed phylogenetic relationships. This study examines the morphological variation of hindwings based on 19 landmarks, 119 morphological characters, and 81 beetle species. Only one most parsimonious tree (MPT) was found based on 119 wing and body characters. To better understand the possible role of the hindwing in the evolution of Scarabaeinae, additional phylogenetic analyses were proposed based on the only body features (106 characters, wing characters excluded). Two MPT were found based on 106 body characters, and five nodes were collapsed in a strict consensus. There was a strong correlation between the morphometric tree and all phylogenetic trees (r>0.5). Reconstructions of the ancestral wing forms suggest that Scarabaeinae hindwing morphology has not changed substantially over time, but the morphological changes that do occur are focused at the base of the wing. These results suggest that flight has been important since the origin of Scarabaeinae, and that variation in hindwing morphology has been limited by functional constraints. Comparison of metric disparity values and relative evolutionary sequences among Scarabaeinae tribes suggest that the primitive dung beetles had relatively diverse hindwing morphologies, while advanced dung beetles have relatively similar wing morphologies. The strong correlation between the morphometric tree and phylogenetic trees suggest that hindwing features reflect the evolution of whole body morphology and that wing characters are suitable for the phylogenetic analyses. By integrating morphometric and cladistic approaches, this paper sheds new light on the evolution of dung beetle hind wings.     

Population differences in density and resource allocation of ornamental tail feathers in the barn swallow

Many organisms show well‐defined latitudinal clines in morphology, which appear to be caused by spatially varying natural selection, resulting in different optimal phenotypes in each location. Such spatial variability raises an interesting question, with different prospects for the action of sexual selection on characters that have a dual purpose, such as locomotion and sexual attraction. The outermost tail feathers of barn swallows (Hirundo rustica) represent one such character, and their evolution has been a classic model subject to intense debate. In the present study, we examined individuals from four European populations to analyze geographical variation in the length and mass of tail feathers in relation to body size and wing size. Tail feather length differed between sexes and populations, and such variation was a result of the effects of natural selection, acting through differences in body size and wing size, as well as the effects of sexual selection that favours longer tails. The extra enlargement of the tail promoted by sexual selection (i.e. beyond the natural selection optimum) could be achieved by increasing investment in ornaments, and by modifying feather structure to produce longer feathers of lower density. These two separate processes accounting for the production of longer and more costly tail feathers and less dense feathers, respectively, are consistent with the hypothesis that both Zahavian and Fisherian mechanisms may be involved in the evolution of the long tails of male barn swallows. We hypothesize that the strength of sexual selection increases with latitude because of the need for rapid mating as a result of the short duration of the breeding season at high latitudes. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 925–936.     

Short stature in African pygmies is not explained by sexual selection

African pygmies' short stature has been studied for more than a century, but the evolution of this extreme phenotype remains unknown. The present study tests the hypothesis that sexual selection, through preference for short partners, may have contributed to the evolution of pygmies' stature. We gathered anthropometric and familial data from 72 Baka pygmy couples and 27 neighboring Nzimé nonpygmy couples from Cameroon. We found evidence for positive assortative mating and partial evidence for the male-taller norm in both groups. This is surprisingly close to results reported for many modern occidental populations, in which sexual selection is thought to exert a positive selective pressure on men height. Semistructured interviews of Baka pygmies concerning height and mate choice suggested that the male-taller norm matches mating preferences. Stature was also positively correlated with the number of serial marriages contracted by men of both populations, while the stature of women was not related to their mating success. Finally, we did not detect any linear or quadratic effect of height on reproductive success for either men or women. Altogether, our results demonstrate that stature influences mate choice in pygmies, and we argue that, if of any influence for sexual selection, mate choice should have favored tallness rather than shortness in our pygmy population. Consequently, this study establishes that sexual selection is a very unlikely candidate to account for the evolution of pygmies' short stature.     

Multivariate stabilizing sexual selection and the evolution of male and female genital morphology in the red flour beetle*

Male genitals are highly divergent in animals with internal fertilization. Most studies attempting to explain this diversity have focused on testing the major hypotheses of genital evolution (the lock-and-key, pleiotropy, and sexual selection hypotheses), and quantifying the form of selection targeting male genitals has played an important role in this endeavor. However, we currently know far less about selection targeting female genitals or how male and female genitals interact during mating. Here, we use formal selection analysis to show that genital size and shape is subject to strong multivariate stabilizing sexual selection in both sexes of the red flour beetle, Tribolium castaneum. Moreover, we show significant sexual selection on the covariance between the sexes for specific aspects of genital shape suggesting that male and female genitalia also interact to determine the successful transfer of a spermatophore during mating. Our work therefore highlights the important role that both male and female genital morphologies play in determining mating success and that these effects can occur independently, as well as through their interaction. Moreover, it cautions against the overly simplistic view that the sexual selection targeting genital morphology will always be directional in form and restricted primarily to males.     

The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies

Abstract Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle , divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle . However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.